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Effect of swallowing training on dysphagia and depression in postoperative tongue cancer patients
European Journal of Oncology Nursing 18 (2014) 626e629
Contents lists available at ScienceDirect
European Journal of Oncology Nursing journal homepage: www.elsevier.com/locate/ejon
Effect of swallowing training on dysphagia and depression in postoperative tongue cancer patients Liping Zhang 1, Zhuoshan Huang 1, Hong Wu, Weiliang Chen, Zhiquan Huang* Department of Oral and Maxillofacial Surgery, Sun Yat-sen Memorial Hospital, Sun Yat-sen University, No.107 Yan Jiang Xi Road, Guangzhou 510120, Guangdong, China
a b s t r a c t Keywords: Dysphagia Depression Swallowing training Tongue cancer Postoperative
Purpose: The aim of the present study was to evaluate the effect of swallowing training on dysphagia and depression in postoperative tongue cancer patients. Method: Fifty-eight tongue cancer patients aged 45e81 years participated in the present study. All patients were scheduled to undergo partial tongue resection and flap rehabilitation. Changes in dysphagia and depression before and after swallowing training were measured. The water swallow test (WST) and the Zung Self-Rating Depression Scale (SDS) were used to evaluate the severity of dysphagia and depression, respectively. Results: The WST level and SDS scores in the less than 50% tongue resection and rehabilitation group were significantly lower than those of the greater than 50% group. The WST level and SDS scores of the early tumor stage group were significantly lower than those of the advanced tumor stage group. WST levels and SDS scores before swallowing training were significantly greater than those measured after swallowing training. In all cases, lower WST levels were associated with lower SDS scores. Conclusions: Postoperative dysphagia, depression and anxiety were improved after swallowing training. Early identification and management of dysphagia can improve treatment outcomes and reduce depression. © 2014 Elsevier Ltd. All rights reserved.
Introduction Dysphagia occurs in up to 50% of head and neck cancer survivors and an estimated 10,000e20,000 new cases are diagnosed annually in the USA (Kazi et al., 2008), particularly in patients with oral cavity and oropharyngeal cancers (Pauloski et al., 2006). Patients with tongue cancer are at high risk for oropharyngeal dysphagia (OD) after surgery. Dysphagia is a growing concern in patients with tongue cancer and can lead to malnutrition, dehydration, weight loss, reduced functional abilities, and fear of eating and drinking; these factors may lead to depression and reduced quality of life (QOL)（Gaziano, 2002.）. Early identification and management of dysphagia may improve treatment outcomes and reduce depression. The recovery of swallowing is integral to the rehabilitation of surgical tongue
* Corresponding author. Tel.: þ86 2081332220; fax: þ86 2081332833. E-mail addresses: [email protected], [email protected] (Z. Huang). 1 The first two authors Liping Zhang and Zhuoshan Huang equally contributed to this work. http://dx.doi.org/10.1016/j.ejon.2014.06.003 1462-3889/© 2014 Elsevier Ltd. All rights reserved.
cancer patients; however, recovery is very slow and often incomplete following treatment (Nicoletti et al., 2004). Videofluoroscopic swallowing examination (VFSE) is often used to determine the extent of dysphagia and is considered to be the gold standard to evaluate dysphagia. VFSE may be used to observe some cases of dysphagia that could not be identified clinically and distinguish the structural and functional aspects of dysphagia. VFSE results may inform swallowing training protocol selection and can be used to track its therapeutic efficacy (Butler et al., 2009; Kendall et al., 2000; Leonard et al., 2000; Kendall et al., 2004). Nevertheless, VFSE has its shortcomings: patients must be transferred to the radiology department, and there are multiple postoperative contraindications to the examination. In the present study, the water swallowing test (WST) was used to evaluate the severity of dysphagia. The WST is a quick and easily administered assessment to diagnose patients with aspiration. This test is a useful adjunct to clinical examination because it helps identify patients who require additional assessment, such as videofluoroscopy. Furthermore, quantitative measures are derived from this test, which can be used to measure swallow performance over time (Patterson et al., 2011). This study was performed to evaluate the efficacy of an interdisciplinary swallowing therapy protocol administered by
L. Zhang et al. / European Journal of Oncology Nursing 18 (2014) 626e629
well-trained nursing professionals to improve swallowing and depression in patients after tongue surgery for squamous cell cancer. Materials and methods
627
rehabilitation physician, and swallowing therapy was administered by the rehabilitation nurse. All data were collected at the beginning of the study and at the end of 1 week of swallowing training. However, to prevent any changes in behavior of the rehabilitation nurse at the time of the study, rehabilitation unit managers were not contacted.
Selection of research sample Water swallow test A prospective study was designed to evaluate swallowing function and depression to determine the efficacy of swallowing exercises. Subjects who met the following inclusion criteria were eligible for participation: (1) those who had undergone tongue resection and rehabilitation; (2) remained conscious after surgery and able to participate in swallowing training; (3) were receiving nutrition and hydration via oral intake; (4) water swallow tests level Ⅱ to Ⅴ prior to training; and (5) able to understand Mandarin or Chinese dialect. Between March 2010 and December 2013, 82 of 128 tongue cancer patients who underwent tongue resection and rehabilitation were diagnosed with dysphagia. Of these dysphagia patients, 58 were selected for the present study. Each subject and their family gave informed consent prior to enrollment and received compensation for participation. Each subject was a patient of the Department of Oral and Maxillofacial Surgery of the Sun Yat-sen Memorial Hospital of Sun Yat-sen University, Guangzhou, China. This study was approved and reviewed by the Institutional Review Board of the Sun Yat-sen Memorial Hospital of Sun Yat-sen University. Subjects were aged 40e81 years (median, 56.6 years); 43 patients were male, and 15 were female. Clinically, 9, 23, 21, and 5 patients were diagnosed with stage I, II, III, and IV cancer, respectively. Of the 58 subjects, 12 exhibited tumors located on the floor of the tongue, 27 on the side of the tongue, 6 near the throat, and 13 on the top of the tongue. Eleven patients underwent segmental mandibular resection in continuity, and the remaining patients underwent resection of the mandibular rim only. The extent of tongue resection varied between 10% and 75%. All histological evaluations indicated squamous cell carcinoma and with tumor-free margins. In subtotal glossectomy patients, hypoglossal and lingual nerves were resected on the affected side but preserved on the contralateral side. Bilateral hypoglossal and lingual nerves were resected in total glossectomy patients. Laryngeal suspension and cricopharyngeal myotomy procedures were based on the following 2 criteria: (1) excision of the bilateral suprahyoid muscles; and (2) excision of 50% or more of the base of the tongue. Research procedure All members of the expert team agreed with the training protocol and received 30-min general swallowing therapy sessions for 10 days. The expert team consisted of a rehabilitation physician, a rehabilitation nurse, and a speech therapist from the Department of Rehabilitation in the Department of Oral and Maxillofacial Surgery, Sun Yat-sen Memorial Hospital of Sun Yat-sen University, Guangzhou, China. The rehabilitation nurse had greater than 5 years of clinical experience in hospital surgical units and underwent 3 months of clinical training for swallowing therapy for dysphagic patients to ensure competence in the screening and management of swallowing problems. The rehabilitation nurse completed a water swallow test before and after the training to assess baseline knowledge, skill, and confidence in dysphagia concepts and treatment. The rehabilitation nurse's training and questionnaire were administered by a speech therapist and the speech therapist performing the training protocol. Subject data were collected by the
For the water swallow test, patients were asked to sit up straight while drinking 30 ml of warm water. The WST was timed and the number of swallows required to drink the entire 30 ml was recorded. Simultaneous phenomena, such as obstructive cough or choking, were observed and recorded. The following classification criteria were used to describe swallowing ability: (1) swallowing all water smoothly in 1 swallow was level Ⅰ; (2) swallowing all water smoothly in 2 or more swallows without bucking was levelⅡ; (3) swallowing all water in 1 swallow with bucking was level Ⅲ; (4) swallowing all water smoothly in 2 or more swallows with bucking was level Ⅳ; (5) being unable to swallow all water and with much bucking was level Ⅴ. The evaluation criterion for normal swallowing is drinking all water within 5 s; levels I and Ⅱ indicate doubtful dysphagia, while levels Ⅲ, Ⅳ and Ⅴ indicate positive dysphagia. Subjects of level Ⅰneed further examination, such as VSFE, to discriminate dysphagia from normal swallowing. Subjects of levels Ⅱ, Ⅲ, Ⅳ and Ⅴ participated in this study. Zung Self-Rating Depression Scale The Zung Self-Rating Depression Scale (SDS) was used to evaluate the severity of depression in the present study (Carroll et al., 1973). The period of time considered when using the SDS spans one week, and it can be used to diagnose depression simply and definitely via analysis of depressive symptomatology. Each patient completed the Zung Self-Rating Depression Scale, which evaluates 10 positive symptoms and 10 negative symptoms, before and after swallowing training (Carroll et al., 1973). The standardized score is equal to 1.25 times the total score. Subjects were classified according to the standardized score: normal- scores below 50; mild depression- scores ranging from 50 to 59 scores; moderate depression- scores ranging from 60 to 69 scores; severe depression- scores between 70-90. Swallowing training protocol The swallowing training protocol was designed based on a literature review and the experience of the research team. The protocol included direct and indirect therapies. Direct therapy typically focuses on the particular tasks or skills to be learned, and included compensatory strategies such as diet modification, environmental arrangement, positioning (including chin-down posture and head rotation), as well as feeding and compensatory swallowing strategies, including the Mendelsohn maneuver and supraglottic and effortful swallowing. Compensatory training may teach patients to use strategies further reduce the risk of aspiration. These strategies may be the only option for patients who continue feed by mouth. For example, a chin-tuck strategy is commonly recommended. This strategy places the epiglottis, a cartilaginous flap located immediately above the larynx, in a more forward position to allow for improved airway protection during swallowing. A head turn may be beneficial for patients with unilateral vocal fold paralysis to improve vocal fold closure when swallowing or for patients with hemiparesis affecting movement of the bolus on one side of the throat.
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L. Zhang et al. / European Journal of Oncology Nursing 18 (2014) 626e629
The Mendelsohn maneuver raises the larynx and opens the esophagus when swallowing, supraglottic swallowing offers laryngeal protection, and effortful swallowing increases pharyngeal constriction and reduces pharyngeal residue. Indirect therapy focuses on treating underlying neurological dysfunction, with the hope that improved neurologic swallowing function will transfer to skill attainment. The indirect therapies used in this study included physical maneuvers and thermal stimulation. Thermal stimulation was used in patients with delayed triggering of the swallowing reflex. Physical maneuvers included lip and lingual exercises. Oral motor exercises (lip, cheek, lingual, and laryngeal exercises) were used for subjects exhibiting oral motor weakness or incoordination. Statistical analysis The KruskaleWallis rank sum test was performed to compare differences in WST level before and after swallowing training according to age, extent of tongue resection and rehabilitation, flap defect rehabilitation, neck dissection, range of mandibulectomy and tumor stage. The Wilcoxon rank sum test was used to compare differences in Zung SDS standardized scores (the same level Ⅱ/Ⅳ patients were ranked by swallowing time, and the same level Ⅲ/Ⅴ patients were ranked by bucking situation) before and after swallowing training according to the same criteria described above. Pvalues less than 0.05 were considered statistically significant. Results The WST and SDS data are presented in Table 1. The WST level and SDS scores in the less than 50% tongue resection and rehabilitation group were significantly lower than those of the greater than 50% group. The WST level and SDS scores of the early tumor stage group were significantly lower than those of the advanced tumor stage group.
There were no significant differences observed in the WST level and SDS score based on age, flap defect rehabilitation, neck dissection or range of mandibulectomy. WST levels and SDS scores before swallowing training were significantly greater than those measured after swallowing training. In all cases, lower WST levels were associated with lower SDS scores. Discussion Oncology traditionally focuses on curing patients. Unfortunately, the cure-centered focus has sometimes resulted in neglecting functional outcomes and patient QOL. Although curing must clearly remain the major goal of treatment, the aforementioned outcomes are equally important. Dysphagia is a common, debilitating and potentially life-threatening sequela of head and neck malignancy. The secondary effects of dysphagia include malnutrition, dehydration, weight loss, functional decline, and fear of eating and drinking, which may lead to depression and reduced QOL. Many factors may affect swallowing in postoperative tongue cancer patients. In the present study, we attempted to analyze these factors to guide clinical swallowing training protocols. The tongue and soft palate are the most important organs in the oral cavity and oropharynx for speech and swallowing. Regarding speech and swallowing, patients who underwent 3/4 or total anterior glossectomy had poorer outcomes than those who underwent either 1/4 or 1/2 glossectomy (Brown et al., 2006). Similar results were obtained in the present study. The mandible and maxilla are static structures that can be replaced with vascularized bone to restore both the form and function of the ablated tissues (Brown, 2008). Appropriate replacement of ablated tissue via free tissue transfer greatly improves functional and QOL outcomes. However, there was no significant difference in swallowing between the free flap and pedicled flap subgroups; this finding has
Table 1 Water swallowing test level and Zung Self-Rating Depression Scale score before and after swallowing training. WST
Age 60 years (n ¼ 27) ＜60 years (n ¼ 31) Tongue resection and rehabilitation ＜50% (n ¼ 30) 50% (n ¼ 28) Flap Free flap (n ¼ 22) Pedicled flap (n ¼ 36) Neck dissection Unilateral (n ¼ 28) Bilateral (n ¼ 30) Mandibulectomy resection Segmental (n ¼ 23) Marginal/preserved (n ¼ 35) Tumor stage Ⅰ (n ¼ 9) Ⅱ (n ¼ 23) Ⅲ (n ¼ 21) Ⅳ (n ¼ 5)
SDS
Before (Ⅱ/Ⅲ/Ⅳ/Ⅴ)
After (Ⅰ/Ⅱ/Ⅲ/Ⅳ)
4/7/14/2 7/12/10/2
7/19/0/1 14/14/3/0
p**
Before
After
p***
75.8 ± 6.3 78.6 ± 5.8
56.7 ± 5.4 54.6 ± 6.1
0.067*
0.304*
0.037* 5/13/12/0 6/6/12/4
12/18/0/0 9/15/3/1
4/8/9/2 7/11/15/2
9/11/1/1 12/22/2/0
4/9/13/2 7/10/11/2
10/18/0/0 11/15/3/1
4/7/11/1 7/12/13/3
9/12/2/0 12/21/1/1
5/3/1/0 3/10/9/1 3/6/11/1 0/0/3/2
9/0/0/0 7/16/0/0 5/15/1/0 0/2/2/1
0.042* 63.6 ± 3.9 80.0 ± 4.7
52.1 ± 6.7 55.6 ± 6.6
68.9 ± 7.4 72.6 ± 5.5
53.3 ± 4.8 56.9 ± 6.5
69.5 ± 3.2 71.5 ± 5.1
54.4 ± 5.4 56.2 ± 5.3
67.8 ± 3.8 72.3 ± 3.2
53.6 ± 4.5 57.2 ± 5.2
0.055*
0.074*
0.078*
0.126*
0.056*
0.062*
0.042*
0.031* 56.7 68.8 73.2 82.3
± ± ± ±
2.1 2.6 4.2 2.3
51.3 58.4 60.5 69.2
± ± ± ±
2.2 3.9 5.7 3.1
WST ¼ water swallowing test level; SDS ¼ standardized score of Zung Self-rating Depression Scale; Before ¼ before swallowing training; After ¼ after swallowing training. *p-value between different subgroups before swallowing training/postoperatively. ** The WST level before swallowing training compared to that after swallowing training, p ¼ 0.027. *** The standardized score of the SDS before swallowing training compared to that after swallowing training, p ¼ 0.034.
L. Zhang et al. / European Journal of Oncology Nursing 18 (2014) 626e629
been previously reported (de Vicente et al., 2008). So long as the tissue is replaced and contraction is avoided, the detrimental effects on functional outcomes are limited. Free flaps can provide vascularized and sensitized skin cover to increase the rate of healing and avoid contraction of the remaining tissues; however, they cannot replace the complex muscular movements of the tongue and soft palate (Brown et al., 2006). Therefore, organ preservation appears to translate to functional preservation, at least in tongue cancer. These findings objectively support recommendations for concurrent swallowing therapy as the treatment of choice in cases of tongue cancer, especially in stages III and IV. Accumulating evidence suggests that learning novel motor skills leads to significant changes in corticomotor control. Appropriate swallowing treatments may reduce complications related to impaired swallowing. Several reviews have detailed the neuroanatomical pathways involved in the control of the tongue musculature (Miller, 2002; Sawczuk and Mosier, 2001), and a series of studies using intracortical microstimulation in conscious monkeys have been systematically discussed. Recently, several studies involving swallowing have been reported. There is increasing evidence for the effectiveness of different treatments, such as direct dysphagia treatment, compensatory training (Lin et al., 2003), electrical stimulation, and the Mendelsohn maneuver (Peck et al., 2010). The current swallowing training protocol included direct and indirect therapies. After ten days of postoperative training, all patients demonstrated significant improvements in swallowing. Early diagnosis and treatment of dysphagia may improve patients' QOL. In the present study, an interesting phenomenon was observed involving factors that simultaneously affect the WST level and Zung SDS score. Swallowing training-related changes in the WST tended to co-occur with SDS scores in the same direction. Thus, improved swallowing may reduce the severity of depression in postoperative dysphagic tongue cancer patients. It is possible that latent mitigation of depression may improve swallowing. The interaction between swallowing and the presence and severity of depression warrant further study. Applying nursing intervention on oral cancer patients can improve their QOL, especially in the emotional function (Hammerlid et al., 1999). In this study, the postoperative tongue cancer patients were actively carried out early swallowing functional training, evaluated the severity of dysphagia and depression by WST and the Zurg SDS, respectively. The results show that early swallowing functional training could improve the swallowing function the patients' psychological state. It's helpful to patients' recovery after operation, improve the QOL. Preliminary research indicates that this method is simple, safe and effective, worthy of promotion in clinical work. Study limitations Although this study confirmed the effectiveness of early diagnosis and swallowing training in improving swallowing functions and depression level, there were several limitations. First, the number of patients was relatively small. As the results, there was not enough sample size for analysis some intervening variables such as gender, tumor size and location. Second, we did not use video fluoroscopy to diagnose swallowing disorders, but instead used WST which is usually used for dysphagia screening. Third, swallowing training-related changes in the WST in this study tended to co-occur with SDS scores in the same direction. However, the causal relationship between them need further study. Forth, it's a short time physiological intervention in patients in the short-term
629
observation, and a long-time training and long-term observation need further studies. In conclusion, a larger sample and diagnosed with video fluoroscopy, the improvement of experimental design to find out the relationship between swallowing function and depression level need to be done in future studies. Funding This work was supported by a grant from the National Nature Science fund of China (81101592) and Guangdong Province Natural Science Fund (S2013010014794) to Zhi-quan Huang. Conflict of interest statement The authors declare no conflicts of interests. References Brown, J.S., 2008. Reconstruction of the maxilla with loss of the orbital floor and orbital preservation: a case for the iliac crest with internal oblique. Seminars in Plastic Surgery 22, 161e174. Brown, J.S., Rogers, S.N., Lowe, D., 2006. A comparison of tongue and soft palate squamous cell carcinoma treated by primary surgery in terms of survival and quality of life outcomes. International Journal of Oral and Maxillofacial Surgery 35, 208e214. Butler, S.G., Stuart, A., Castell, D., Russell, G.B., Koch, K., Kemp, S., 2009. Effects of age, gender, bolus condition, viscosity, and volume on pharyngeal and upper esophageal sphincter pressure and temporal measurements during swallowing. Journal of Speech, Language, and Hearing Research 52, 240e253. Carroll, B.J., Fielding, J.M., Blashki, T.G., 1973. Depression rating scales. a critical review. Archives of General Psychiatry 28, 361e366. ~ a, I., 2008. Microvascular free tissue de Vicente, J.C., de Villalain, L., Torre, A., Pen transfer for tongue reconstruction after hemiglossectomy: a functional assessment of radial forearm versus anterolateral thigh flap. Journal of Oral and Maxillofacial Surgery 66, 2270e2275. Gaziano, J.E., 2002. Evaluation and management of oropharyngeal dysphagia in head and neck cancer. Cancer Control 9, 400e409. Hammerlid, E., Persson, L.O., Sullivan, M., Westin, T., 1999. Quality-of-life effects of psychosocial intervention in patients with head and neck cancer. Otolaryngology and Head and Neck Surgery 120, 507e616. Kazi, R., Prasad, V., Venkitaraman, R., Nutting, C.M., Clarke, P., Rhys-Evans, P., et al., 2008. Questionnaire analysis of swallowing-related outcomes following glossectomy. Journal for Oto-rhino-Laryngology and its Related Specialties 2008 (70), 151e155. Kendall, K.A., Mckenzie, S., Leonard, R.J., Gonçalves, M.I., Walker, A., 2000. Timing of events in normal swallowing: a videofluoroscopic study. Dysphagia 15, 74e83. Kendall, K.A., Leonard, R.J., Mckenzie, S., 2004. Airway protection: evaluation with videofluoroscopy. Dysphagia 19, 65e70. Leonard, R.J., Kendall, K.A., Mckenzie, S., Gonçalves, M.I., Walker, A., 2000. Structural displacements in normal swallowing: a videofluoroscopic study. Dysphagia 15, 146e152. Lin, L.C., Wang, S.C., Chen, S.H., Wang, T.G., Chen, M.Y., Wu, S.C., 2003. Efficacy of swallowing training for residents following stroke. Journal of Advanced Nursing 44, 469e478. Miller, A.J., 2002. Oral and pharyngeal reflexes in the mammalian nervous system: their diverse range in complexity and the pivotal role of the tongue. Critical Reviews in Oral Biology and Medicine 13, 409e425. Nicoletti, G., Soutar, D.S., Jackson, M.S., Wrench, A.A., Robertson, G., 2004. Chewing and swallowing after surgical treatment for oral cancer: functional evaluation in 196 selected cases. Plastic and Reconstructive Surgery 114, 329e338. Patterson, J.M., Hildreth, A., McColl, E., Carding, P.N., Hamilton, D., Wilson, J.A., 2011. The clinical application of the 100mL water swallow test in head and neck cancer. Oral Oncology 47, 180e184. Pauloski, B.R., Rademaker, A.W., Logemann, J.A., Newman, L., MacCracken, E., Gaziano, J., et al., 2006. Relationship between swallow motility disorders on videofluorography and oral intake in patients treated for head and neck cancer with radiotherapy with or without chemotherapy. Head and Neck 28, 1069e1076. Peck, K.K., Branski, R.C., Lazarus, C., Cody, V., Kraus, D., Haupage, S., et al., 2010. Cortical activation during swallowing rehabilitation maneuvers: a functional MRI study of healthy controls. Laryngoscope 20, 2153e2159. Sawczuk, A., Mosier, K.M., 2001. Neural control of tongue movement with respect to respiration and swallowing. Critical Reviews in Oral Biology and Medicine 12, 18e37.
Contents lists available at ScienceDirect
European Journal of Oncology Nursing journal homepage: www.elsevier.com/locate/ejon
Effect of swallowing training on dysphagia and depression in postoperative tongue cancer patients Liping Zhang 1, Zhuoshan Huang 1, Hong Wu, Weiliang Chen, Zhiquan Huang* Department of Oral and Maxillofacial Surgery, Sun Yat-sen Memorial Hospital, Sun Yat-sen University, No.107 Yan Jiang Xi Road, Guangzhou 510120, Guangdong, China
a b s t r a c t Keywords: Dysphagia Depression Swallowing training Tongue cancer Postoperative
Purpose: The aim of the present study was to evaluate the effect of swallowing training on dysphagia and depression in postoperative tongue cancer patients. Method: Fifty-eight tongue cancer patients aged 45e81 years participated in the present study. All patients were scheduled to undergo partial tongue resection and flap rehabilitation. Changes in dysphagia and depression before and after swallowing training were measured. The water swallow test (WST) and the Zung Self-Rating Depression Scale (SDS) were used to evaluate the severity of dysphagia and depression, respectively. Results: The WST level and SDS scores in the less than 50% tongue resection and rehabilitation group were significantly lower than those of the greater than 50% group. The WST level and SDS scores of the early tumor stage group were significantly lower than those of the advanced tumor stage group. WST levels and SDS scores before swallowing training were significantly greater than those measured after swallowing training. In all cases, lower WST levels were associated with lower SDS scores. Conclusions: Postoperative dysphagia, depression and anxiety were improved after swallowing training. Early identification and management of dysphagia can improve treatment outcomes and reduce depression. © 2014 Elsevier Ltd. All rights reserved.
Introduction Dysphagia occurs in up to 50% of head and neck cancer survivors and an estimated 10,000e20,000 new cases are diagnosed annually in the USA (Kazi et al., 2008), particularly in patients with oral cavity and oropharyngeal cancers (Pauloski et al., 2006). Patients with tongue cancer are at high risk for oropharyngeal dysphagia (OD) after surgery. Dysphagia is a growing concern in patients with tongue cancer and can lead to malnutrition, dehydration, weight loss, reduced functional abilities, and fear of eating and drinking; these factors may lead to depression and reduced quality of life (QOL)（Gaziano, 2002.）. Early identification and management of dysphagia may improve treatment outcomes and reduce depression. The recovery of swallowing is integral to the rehabilitation of surgical tongue
* Corresponding author. Tel.: þ86 2081332220; fax: þ86 2081332833. E-mail addresses: [email protected], [email protected] (Z. Huang). 1 The first two authors Liping Zhang and Zhuoshan Huang equally contributed to this work. http://dx.doi.org/10.1016/j.ejon.2014.06.003 1462-3889/© 2014 Elsevier Ltd. All rights reserved.
cancer patients; however, recovery is very slow and often incomplete following treatment (Nicoletti et al., 2004). Videofluoroscopic swallowing examination (VFSE) is often used to determine the extent of dysphagia and is considered to be the gold standard to evaluate dysphagia. VFSE may be used to observe some cases of dysphagia that could not be identified clinically and distinguish the structural and functional aspects of dysphagia. VFSE results may inform swallowing training protocol selection and can be used to track its therapeutic efficacy (Butler et al., 2009; Kendall et al., 2000; Leonard et al., 2000; Kendall et al., 2004). Nevertheless, VFSE has its shortcomings: patients must be transferred to the radiology department, and there are multiple postoperative contraindications to the examination. In the present study, the water swallowing test (WST) was used to evaluate the severity of dysphagia. The WST is a quick and easily administered assessment to diagnose patients with aspiration. This test is a useful adjunct to clinical examination because it helps identify patients who require additional assessment, such as videofluoroscopy. Furthermore, quantitative measures are derived from this test, which can be used to measure swallow performance over time (Patterson et al., 2011). This study was performed to evaluate the efficacy of an interdisciplinary swallowing therapy protocol administered by
L. Zhang et al. / European Journal of Oncology Nursing 18 (2014) 626e629
well-trained nursing professionals to improve swallowing and depression in patients after tongue surgery for squamous cell cancer. Materials and methods
627
rehabilitation physician, and swallowing therapy was administered by the rehabilitation nurse. All data were collected at the beginning of the study and at the end of 1 week of swallowing training. However, to prevent any changes in behavior of the rehabilitation nurse at the time of the study, rehabilitation unit managers were not contacted.
Selection of research sample Water swallow test A prospective study was designed to evaluate swallowing function and depression to determine the efficacy of swallowing exercises. Subjects who met the following inclusion criteria were eligible for participation: (1) those who had undergone tongue resection and rehabilitation; (2) remained conscious after surgery and able to participate in swallowing training; (3) were receiving nutrition and hydration via oral intake; (4) water swallow tests level Ⅱ to Ⅴ prior to training; and (5) able to understand Mandarin or Chinese dialect. Between March 2010 and December 2013, 82 of 128 tongue cancer patients who underwent tongue resection and rehabilitation were diagnosed with dysphagia. Of these dysphagia patients, 58 were selected for the present study. Each subject and their family gave informed consent prior to enrollment and received compensation for participation. Each subject was a patient of the Department of Oral and Maxillofacial Surgery of the Sun Yat-sen Memorial Hospital of Sun Yat-sen University, Guangzhou, China. This study was approved and reviewed by the Institutional Review Board of the Sun Yat-sen Memorial Hospital of Sun Yat-sen University. Subjects were aged 40e81 years (median, 56.6 years); 43 patients were male, and 15 were female. Clinically, 9, 23, 21, and 5 patients were diagnosed with stage I, II, III, and IV cancer, respectively. Of the 58 subjects, 12 exhibited tumors located on the floor of the tongue, 27 on the side of the tongue, 6 near the throat, and 13 on the top of the tongue. Eleven patients underwent segmental mandibular resection in continuity, and the remaining patients underwent resection of the mandibular rim only. The extent of tongue resection varied between 10% and 75%. All histological evaluations indicated squamous cell carcinoma and with tumor-free margins. In subtotal glossectomy patients, hypoglossal and lingual nerves were resected on the affected side but preserved on the contralateral side. Bilateral hypoglossal and lingual nerves were resected in total glossectomy patients. Laryngeal suspension and cricopharyngeal myotomy procedures were based on the following 2 criteria: (1) excision of the bilateral suprahyoid muscles; and (2) excision of 50% or more of the base of the tongue. Research procedure All members of the expert team agreed with the training protocol and received 30-min general swallowing therapy sessions for 10 days. The expert team consisted of a rehabilitation physician, a rehabilitation nurse, and a speech therapist from the Department of Rehabilitation in the Department of Oral and Maxillofacial Surgery, Sun Yat-sen Memorial Hospital of Sun Yat-sen University, Guangzhou, China. The rehabilitation nurse had greater than 5 years of clinical experience in hospital surgical units and underwent 3 months of clinical training for swallowing therapy for dysphagic patients to ensure competence in the screening and management of swallowing problems. The rehabilitation nurse completed a water swallow test before and after the training to assess baseline knowledge, skill, and confidence in dysphagia concepts and treatment. The rehabilitation nurse's training and questionnaire were administered by a speech therapist and the speech therapist performing the training protocol. Subject data were collected by the
For the water swallow test, patients were asked to sit up straight while drinking 30 ml of warm water. The WST was timed and the number of swallows required to drink the entire 30 ml was recorded. Simultaneous phenomena, such as obstructive cough or choking, were observed and recorded. The following classification criteria were used to describe swallowing ability: (1) swallowing all water smoothly in 1 swallow was level Ⅰ; (2) swallowing all water smoothly in 2 or more swallows without bucking was levelⅡ; (3) swallowing all water in 1 swallow with bucking was level Ⅲ; (4) swallowing all water smoothly in 2 or more swallows with bucking was level Ⅳ; (5) being unable to swallow all water and with much bucking was level Ⅴ. The evaluation criterion for normal swallowing is drinking all water within 5 s; levels I and Ⅱ indicate doubtful dysphagia, while levels Ⅲ, Ⅳ and Ⅴ indicate positive dysphagia. Subjects of level Ⅰneed further examination, such as VSFE, to discriminate dysphagia from normal swallowing. Subjects of levels Ⅱ, Ⅲ, Ⅳ and Ⅴ participated in this study. Zung Self-Rating Depression Scale The Zung Self-Rating Depression Scale (SDS) was used to evaluate the severity of depression in the present study (Carroll et al., 1973). The period of time considered when using the SDS spans one week, and it can be used to diagnose depression simply and definitely via analysis of depressive symptomatology. Each patient completed the Zung Self-Rating Depression Scale, which evaluates 10 positive symptoms and 10 negative symptoms, before and after swallowing training (Carroll et al., 1973). The standardized score is equal to 1.25 times the total score. Subjects were classified according to the standardized score: normal- scores below 50; mild depression- scores ranging from 50 to 59 scores; moderate depression- scores ranging from 60 to 69 scores; severe depression- scores between 70-90. Swallowing training protocol The swallowing training protocol was designed based on a literature review and the experience of the research team. The protocol included direct and indirect therapies. Direct therapy typically focuses on the particular tasks or skills to be learned, and included compensatory strategies such as diet modification, environmental arrangement, positioning (including chin-down posture and head rotation), as well as feeding and compensatory swallowing strategies, including the Mendelsohn maneuver and supraglottic and effortful swallowing. Compensatory training may teach patients to use strategies further reduce the risk of aspiration. These strategies may be the only option for patients who continue feed by mouth. For example, a chin-tuck strategy is commonly recommended. This strategy places the epiglottis, a cartilaginous flap located immediately above the larynx, in a more forward position to allow for improved airway protection during swallowing. A head turn may be beneficial for patients with unilateral vocal fold paralysis to improve vocal fold closure when swallowing or for patients with hemiparesis affecting movement of the bolus on one side of the throat.
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The Mendelsohn maneuver raises the larynx and opens the esophagus when swallowing, supraglottic swallowing offers laryngeal protection, and effortful swallowing increases pharyngeal constriction and reduces pharyngeal residue. Indirect therapy focuses on treating underlying neurological dysfunction, with the hope that improved neurologic swallowing function will transfer to skill attainment. The indirect therapies used in this study included physical maneuvers and thermal stimulation. Thermal stimulation was used in patients with delayed triggering of the swallowing reflex. Physical maneuvers included lip and lingual exercises. Oral motor exercises (lip, cheek, lingual, and laryngeal exercises) were used for subjects exhibiting oral motor weakness or incoordination. Statistical analysis The KruskaleWallis rank sum test was performed to compare differences in WST level before and after swallowing training according to age, extent of tongue resection and rehabilitation, flap defect rehabilitation, neck dissection, range of mandibulectomy and tumor stage. The Wilcoxon rank sum test was used to compare differences in Zung SDS standardized scores (the same level Ⅱ/Ⅳ patients were ranked by swallowing time, and the same level Ⅲ/Ⅴ patients were ranked by bucking situation) before and after swallowing training according to the same criteria described above. Pvalues less than 0.05 were considered statistically significant. Results The WST and SDS data are presented in Table 1. The WST level and SDS scores in the less than 50% tongue resection and rehabilitation group were significantly lower than those of the greater than 50% group. The WST level and SDS scores of the early tumor stage group were significantly lower than those of the advanced tumor stage group.
There were no significant differences observed in the WST level and SDS score based on age, flap defect rehabilitation, neck dissection or range of mandibulectomy. WST levels and SDS scores before swallowing training were significantly greater than those measured after swallowing training. In all cases, lower WST levels were associated with lower SDS scores. Discussion Oncology traditionally focuses on curing patients. Unfortunately, the cure-centered focus has sometimes resulted in neglecting functional outcomes and patient QOL. Although curing must clearly remain the major goal of treatment, the aforementioned outcomes are equally important. Dysphagia is a common, debilitating and potentially life-threatening sequela of head and neck malignancy. The secondary effects of dysphagia include malnutrition, dehydration, weight loss, functional decline, and fear of eating and drinking, which may lead to depression and reduced QOL. Many factors may affect swallowing in postoperative tongue cancer patients. In the present study, we attempted to analyze these factors to guide clinical swallowing training protocols. The tongue and soft palate are the most important organs in the oral cavity and oropharynx for speech and swallowing. Regarding speech and swallowing, patients who underwent 3/4 or total anterior glossectomy had poorer outcomes than those who underwent either 1/4 or 1/2 glossectomy (Brown et al., 2006). Similar results were obtained in the present study. The mandible and maxilla are static structures that can be replaced with vascularized bone to restore both the form and function of the ablated tissues (Brown, 2008). Appropriate replacement of ablated tissue via free tissue transfer greatly improves functional and QOL outcomes. However, there was no significant difference in swallowing between the free flap and pedicled flap subgroups; this finding has
Table 1 Water swallowing test level and Zung Self-Rating Depression Scale score before and after swallowing training. WST
Age 60 years (n ¼ 27) ＜60 years (n ¼ 31) Tongue resection and rehabilitation ＜50% (n ¼ 30) 50% (n ¼ 28) Flap Free flap (n ¼ 22) Pedicled flap (n ¼ 36) Neck dissection Unilateral (n ¼ 28) Bilateral (n ¼ 30) Mandibulectomy resection Segmental (n ¼ 23) Marginal/preserved (n ¼ 35) Tumor stage Ⅰ (n ¼ 9) Ⅱ (n ¼ 23) Ⅲ (n ¼ 21) Ⅳ (n ¼ 5)
SDS
Before (Ⅱ/Ⅲ/Ⅳ/Ⅴ)
After (Ⅰ/Ⅱ/Ⅲ/Ⅳ)
4/7/14/2 7/12/10/2
7/19/0/1 14/14/3/0
p**
Before
After
p***
75.8 ± 6.3 78.6 ± 5.8
56.7 ± 5.4 54.6 ± 6.1
0.067*
0.304*
0.037* 5/13/12/0 6/6/12/4
12/18/0/0 9/15/3/1
4/8/9/2 7/11/15/2
9/11/1/1 12/22/2/0
4/9/13/2 7/10/11/2
10/18/0/0 11/15/3/1
4/7/11/1 7/12/13/3
9/12/2/0 12/21/1/1
5/3/1/0 3/10/9/1 3/6/11/1 0/0/3/2
9/0/0/0 7/16/0/0 5/15/1/0 0/2/2/1
0.042* 63.6 ± 3.9 80.0 ± 4.7
52.1 ± 6.7 55.6 ± 6.6
68.9 ± 7.4 72.6 ± 5.5
53.3 ± 4.8 56.9 ± 6.5
69.5 ± 3.2 71.5 ± 5.1
54.4 ± 5.4 56.2 ± 5.3
67.8 ± 3.8 72.3 ± 3.2
53.6 ± 4.5 57.2 ± 5.2
0.055*
0.074*
0.078*
0.126*
0.056*
0.062*
0.042*
0.031* 56.7 68.8 73.2 82.3
± ± ± ±
2.1 2.6 4.2 2.3
51.3 58.4 60.5 69.2
± ± ± ±
2.2 3.9 5.7 3.1
WST ¼ water swallowing test level; SDS ¼ standardized score of Zung Self-rating Depression Scale; Before ¼ before swallowing training; After ¼ after swallowing training. *p-value between different subgroups before swallowing training/postoperatively. ** The WST level before swallowing training compared to that after swallowing training, p ¼ 0.027. *** The standardized score of the SDS before swallowing training compared to that after swallowing training, p ¼ 0.034.
L. Zhang et al. / European Journal of Oncology Nursing 18 (2014) 626e629
been previously reported (de Vicente et al., 2008). So long as the tissue is replaced and contraction is avoided, the detrimental effects on functional outcomes are limited. Free flaps can provide vascularized and sensitized skin cover to increase the rate of healing and avoid contraction of the remaining tissues; however, they cannot replace the complex muscular movements of the tongue and soft palate (Brown et al., 2006). Therefore, organ preservation appears to translate to functional preservation, at least in tongue cancer. These findings objectively support recommendations for concurrent swallowing therapy as the treatment of choice in cases of tongue cancer, especially in stages III and IV. Accumulating evidence suggests that learning novel motor skills leads to significant changes in corticomotor control. Appropriate swallowing treatments may reduce complications related to impaired swallowing. Several reviews have detailed the neuroanatomical pathways involved in the control of the tongue musculature (Miller, 2002; Sawczuk and Mosier, 2001), and a series of studies using intracortical microstimulation in conscious monkeys have been systematically discussed. Recently, several studies involving swallowing have been reported. There is increasing evidence for the effectiveness of different treatments, such as direct dysphagia treatment, compensatory training (Lin et al., 2003), electrical stimulation, and the Mendelsohn maneuver (Peck et al., 2010). The current swallowing training protocol included direct and indirect therapies. After ten days of postoperative training, all patients demonstrated significant improvements in swallowing. Early diagnosis and treatment of dysphagia may improve patients' QOL. In the present study, an interesting phenomenon was observed involving factors that simultaneously affect the WST level and Zung SDS score. Swallowing training-related changes in the WST tended to co-occur with SDS scores in the same direction. Thus, improved swallowing may reduce the severity of depression in postoperative dysphagic tongue cancer patients. It is possible that latent mitigation of depression may improve swallowing. The interaction between swallowing and the presence and severity of depression warrant further study. Applying nursing intervention on oral cancer patients can improve their QOL, especially in the emotional function (Hammerlid et al., 1999). In this study, the postoperative tongue cancer patients were actively carried out early swallowing functional training, evaluated the severity of dysphagia and depression by WST and the Zurg SDS, respectively. The results show that early swallowing functional training could improve the swallowing function the patients' psychological state. It's helpful to patients' recovery after operation, improve the QOL. Preliminary research indicates that this method is simple, safe and effective, worthy of promotion in clinical work. Study limitations Although this study confirmed the effectiveness of early diagnosis and swallowing training in improving swallowing functions and depression level, there were several limitations. First, the number of patients was relatively small. As the results, there was not enough sample size for analysis some intervening variables such as gender, tumor size and location. Second, we did not use video fluoroscopy to diagnose swallowing disorders, but instead used WST which is usually used for dysphagia screening. Third, swallowing training-related changes in the WST in this study tended to co-occur with SDS scores in the same direction. However, the causal relationship between them need further study. Forth, it's a short time physiological intervention in patients in the short-term
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observation, and a long-time training and long-term observation need further studies. In conclusion, a larger sample and diagnosed with video fluoroscopy, the improvement of experimental design to find out the relationship between swallowing function and depression level need to be done in future studies. Funding This work was supported by a grant from the National Nature Science fund of China (81101592) and Guangdong Province Natural Science Fund (S2013010014794) to Zhi-quan Huang. Conflict of interest statement The authors declare no conflicts of interests. References Brown, J.S., 2008. Reconstruction of the maxilla with loss of the orbital floor and orbital preservation: a case for the iliac crest with internal oblique. Seminars in Plastic Surgery 22, 161e174. Brown, J.S., Rogers, S.N., Lowe, D., 2006. A comparison of tongue and soft palate squamous cell carcinoma treated by primary surgery in terms of survival and quality of life outcomes. International Journal of Oral and Maxillofacial Surgery 35, 208e214. Butler, S.G., Stuart, A., Castell, D., Russell, G.B., Koch, K., Kemp, S., 2009. Effects of age, gender, bolus condition, viscosity, and volume on pharyngeal and upper esophageal sphincter pressure and temporal measurements during swallowing. Journal of Speech, Language, and Hearing Research 52, 240e253. Carroll, B.J., Fielding, J.M., Blashki, T.G., 1973. Depression rating scales. a critical review. Archives of General Psychiatry 28, 361e366. ~ a, I., 2008. Microvascular free tissue de Vicente, J.C., de Villalain, L., Torre, A., Pen transfer for tongue reconstruction after hemiglossectomy: a functional assessment of radial forearm versus anterolateral thigh flap. Journal of Oral and Maxillofacial Surgery 66, 2270e2275. Gaziano, J.E., 2002. Evaluation and management of oropharyngeal dysphagia in head and neck cancer. Cancer Control 9, 400e409. Hammerlid, E., Persson, L.O., Sullivan, M., Westin, T., 1999. Quality-of-life effects of psychosocial intervention in patients with head and neck cancer. Otolaryngology and Head and Neck Surgery 120, 507e616. Kazi, R., Prasad, V., Venkitaraman, R., Nutting, C.M., Clarke, P., Rhys-Evans, P., et al., 2008. Questionnaire analysis of swallowing-related outcomes following glossectomy. Journal for Oto-rhino-Laryngology and its Related Specialties 2008 (70), 151e155. Kendall, K.A., Mckenzie, S., Leonard, R.J., Gonçalves, M.I., Walker, A., 2000. Timing of events in normal swallowing: a videofluoroscopic study. Dysphagia 15, 74e83. Kendall, K.A., Leonard, R.J., Mckenzie, S., 2004. Airway protection: evaluation with videofluoroscopy. Dysphagia 19, 65e70. Leonard, R.J., Kendall, K.A., Mckenzie, S., Gonçalves, M.I., Walker, A., 2000. Structural displacements in normal swallowing: a videofluoroscopic study. Dysphagia 15, 146e152. Lin, L.C., Wang, S.C., Chen, S.H., Wang, T.G., Chen, M.Y., Wu, S.C., 2003. Efficacy of swallowing training for residents following stroke. Journal of Advanced Nursing 44, 469e478. Miller, A.J., 2002. Oral and pharyngeal reflexes in the mammalian nervous system: their diverse range in complexity and the pivotal role of the tongue. Critical Reviews in Oral Biology and Medicine 13, 409e425. Nicoletti, G., Soutar, D.S., Jackson, M.S., Wrench, A.A., Robertson, G., 2004. Chewing and swallowing after surgical treatment for oral cancer: functional evaluation in 196 selected cases. Plastic and Reconstructive Surgery 114, 329e338. Patterson, J.M., Hildreth, A., McColl, E., Carding, P.N., Hamilton, D., Wilson, J.A., 2011. The clinical application of the 100mL water swallow test in head and neck cancer. Oral Oncology 47, 180e184. Pauloski, B.R., Rademaker, A.W., Logemann, J.A., Newman, L., MacCracken, E., Gaziano, J., et al., 2006. Relationship between swallow motility disorders on videofluorography and oral intake in patients treated for head and neck cancer with radiotherapy with or without chemotherapy. Head and Neck 28, 1069e1076. Peck, K.K., Branski, R.C., Lazarus, C., Cody, V., Kraus, D., Haupage, S., et al., 2010. Cortical activation during swallowing rehabilitation maneuvers: a functional MRI study of healthy controls. Laryngoscope 20, 2153e2159. Sawczuk, A., Mosier, K.M., 2001. Neural control of tongue movement with respect to respiration and swallowing. Critical Reviews in Oral Biology and Medicine 12, 18e37.